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Obstetrics and Gynegology2024№2
The urinary microbiota in healthy...

The urinary microbiota in healthy pre- and postmenopausal women and its changes in overactive bladder syndrome

DOI
https://dx.doi.org/10.18565/aig.2023.297

Belyi L.E.

Ulyanovsk State University, Ulyanovsk, Russia

The urinary microbiota is similar to other human microbial communities in terms of its organization: there is no single normal state, however, despite serious interindividual differences in composition and diversity, there are some trends in their organization. The composition of the urinary microbiota depends on gender, age, lifestyle, diet, medications taken by a patient, and hormonal status.
This review presents new scientific data on the principles of organizing the urinary microbial community in healthy women. The most common urotypes of the urinary microbiota are described. 
The review shows the results of studies proving the close link of the urinary microbiota with the microbial community of the vagina and gastrointestinal tract. The analysis of the clinical studies demonstrates that the presence of Lactobacillus in the bladder is one of the protective mechanisms of the urinary tract from uropathogens, therefore quantitative and qualitative changes in the urinary microbial community in postmenopausal women are likely to increase the risk of urinary tract diseases.
The results of studies on the role of the urinary microbiota in the development of an overactive bladder syndrome and urgent urinary incontinence are discussed.
Conclusion: It is necessary to continue studying the principles of the organization of the urinary microbiota in a healthy woman and the changes occurring in the urinary microbial community under pathological conditions, since it may contribute to the development of new preventive, diagnostic and therapeutic strategies for a wide variety of diseases.

Conflicts of interest: The author declares lack of the possible conflicts of interests.
Funding: The study was conducted without sponsorship.
For citation: Belyi L.E. The urinary microbiota in healthy pre- and postmenopausal women and its changes in overactive bladder syndrome.
Akusherstvo i Ginekologiya/Obstetrics and Gynecology. 2024; (2): 23-30 (in Russian) 
https://dx.doi.org/10.18565/aig.2023.297

Keywords

urinary microbiota
urotype
postmenopause
overactive bladder
urgent urinary incontinence
Full text (in Russian)

References

  1. Chorbińska J., Krajewski W., Nowak Ł., Małkiewicz B., Del Giudice F., Szydełko T. Urinary microbiome in bladder diseases-review. Biomedicines. 2023; 11(10): 2816. https://dx.doi.org/10.3390/biomedicines11102816.
  2. Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature. 2012; 486(7402): 207-14. https://dx.doi.org/10.1038/nature11234.
  3. Zasloff M. Antimicrobial peptides, innate immunity, and the normally sterile urinary tract. J. Am. Soc. Nephrol. 2007; 18(11): 2810-6. https://dx.doi.org/10.1681/ASN.2007050611.
  4. Слесаревская М.Н., Кузьмин И.В., Жумадиллаев К.Г., Введенский Г.А., Михеев Ю.А., Максимова А.В. Микробиом и микробиота мочи: современные представления и гендерные особенности. Урологические ведомости. 2022; 12(2): 157-65. [Slesarevskaya M.N., Kuzmin I.V., Zhumadillayev K.G., Vvedenskiy G.A., Mikheev Y.А., Maksimova A.V. Microbiome and urine microbiota: modern concepts and gender features. Urology Reports. 2022; 12(2): 157-65. (in Russian)]. https://dx.doi.org/10.17816/uroved109278.
  5. Borgo F., Verduci E., Riva A., Lassandro C., Riva E., Morace G., Borghi E. Relative abundance in bacterial and fungal gut microbes in obese children: a case control study. Child. Obes. 2017; 13(1): 78-84. https://dx.doi.org/10.1089/chi.2015.0194.
  6. Saad M.J., Santos A., Prada P.O. Linking gut microbiota and inflammation to obesity and insulin resistance. Physiology (Bethesda). 2016; 31(4): 283-93. https://dx.doi.org/ 10.1152/physiol.00041.2015.
  7. Kesika P., Suganthy N., Sivamaruthi B.S., Chaiyasut C. Role of gut-brain axis, gut microbial composition, and probiotic intervention in Alzheimer's disease. Life Sci. 2021; 264:118627. https://dx.doi.org/10.1016/j.lfs.2020.118627.
  8. Łoś-Rycharska E., Gołębiewski M., Sikora M., Grzybowski T., Gorzkiewicz M., Popielarz M. et al. Combined analysis of gut and skin microbiota in infants with food allergy and atopic dermatitis: a pilot study. Nutrients. 2021; 13(5): 1682. https://dx.doi.org/10.3390/nu13051682.
  9. Price T.K., Hilt E.E., Thomas-White K., Mueller E.R., Wolfe A.J., Brubaker L. The urobiome of continent adult women: a cross-sectional study. BJOG. 2020; 127(2): 193-201. https://dx.doi.org/10.1111/1471-0528.15920.
  10. Pearce M.M., Hilt E.E., Rosenfeld A.B., Zilliox M.J., Thomas-White K., Fok C. et al. The female urinary microbiome: a comparison of women with and without urgency urinary incontinence. mBio. 2014; 5(4):e01283-14. https://dx.doi.org/10.1128/mBio.01283-14.
  11. Choi H.W., Lee K.W., Kim Y.H. Microbiome in urological diseases: Axis crosstalk and bladder disorders. Investig. Clin. Urol. 2023; 64(2): 126-39. https://dx.doi.org/10.4111/icu.20220357.
  12. Bučević Popović V., Šitum M., Chow C.T., Chan L.S., Roje B., Terzić J. The urinary microbiome associated with bladder cancer. Sci. Rep. 2018; 8(1): 12157. https://dx.doi.org/ 10.1038/s41598-018-29054-w.
  13. Liu F., Ling Z., Xiao Y., Yang Q., Zheng L., Jiang P. et al. Characterization of the urinary microbiota of elderly women and the effects of type 2 diabetes and urinary tract infections on the microbiota. Oncotarget. 2017; 8(59):100678-90. https://dx.doi.org/10.18632/oncotarget.21126.
  14. Perez-Carrasco V., Soriano-Lerma A., Soriano M., Gutiérrez-Fernández J., Garcia-Salcedo J.A. Urinary microbiome: yin and yang of the urinary tract. Front. Cell. Infect. Microbiol. 2021; 11: 617002. https://dx.doi.org/10.3389/fcimb.2021.617002.
  15. Siddiqui H., Nederbragt A.J., Lagesen K., Jeansson S.L., Jakobsen K.S. Assessing diversity of the female urine microbiota by high throughput sequencing of 16S rDNA amplicons. BMC Microbiol. 2011; 11: 244. https://dx.doi.org/10.1186/1471-2180-11-244.
  16. Wolfe A.J., Toh E., Shibata N., Rong R., Kenton K., Fitzgerald M. et al. Evidence of uncultivated bacteria in the adult female bladder. J. Clin. Microbiol. 2012; 50(4): 1376-83. https://dx.doi.org/10.1128/JCM.05852-11.
  17. Wilson M.L., Gaido L. Laboratory diagnosis of urinary tract infections in adult patients. Clin. Infect. Dis. 2004; 38(8): 1150-8. https://dx.doi.org/10.1086/383029.
  18. Hilt E.E., McKinley K., Pearce M.M., Rosenfeld A.B., Zilliox M.J., Mueller E.R. et al. Urine is not sterile: use of enhanced urine culture techniques to detect resident bacterial flora in the adult female bladder. J. Clin. Microbiol. 2014; 52(3): 871-6. https://dx.doi.org/10.1128/JCM.02876-13.
  19. Southworth E., Hochstedler B., Price T.K., Joyce C., Wolfe A.J., Mueller E.R. A cross-sectional pilot cohort study comparing standard urine collection to the peezy midstream device for research studies involving women. Female Pelvic Med. Reconstr. Surg. 2019; 25(2): e28-e33. https://dx.doi.org/10.1097/SPV.0000000000000693.
  20. Thapaliya J., Khadka P., Thapa S., Gongal C. Enhanced quantitative urine culture technique, a slight modification, in detecting under-diagnosed pediatric urinary tract infection. BMC Res. Notes. 2020; 13(1): 5. https://dx.doi.org/10.1186/s13104-019-4875-y.
  21. Modena B.D., Milam R., Harrison F., Cheeseman J.A., Abecassis M.M., Friedewald J.J. et al. Changes in urinary microbiome populations correlate in kidney transplants with interstitial fibrosis and tubular atrophy documented in early surveillance biopsies. Am. J. Transplant. 2017; 17(3): 712-23. https://dx.doi.org/10.1111/ajt.14038.
  22. Коган М.И., Набока Ю.Л., Ибишев Х.С., Гудима И.А. Нестерильность мочи здорового человека - новая парадигма в медицине. Урология. 2014; 5: 48-52. [Kogan M.I., Naboka Yu.L., Ibishev Kh.S., I.A. Gudima I.A. Unsterile urine in health human – new paradigm in medicine. Urologiia. 2014; (5): 48-52. (in Russian)].
  23. Белый Л.Е. Перспективы применения D-маннозы в профилактике и лечении инфекции мочевых путей у женщин. Акушерство и гинекология. 2023; 5: 21-8. [Belyi L.E. Prospects for using D mannose in the prevention and treatment of urinary tract infection in women. Obstetrics and Gynecology. 2023; (5): 21-8. (in Russian)]. https://dx.doi.org/10.18565/aig.2022.295.
  24. Mueller E.R., Wolfe A.J., Brubaker L. Female urinary microbiota. Curr. Opin. Urol. 2017; 27(3): 282-6. https://dx.doi.org/10.1097/MOU.0000000000000396.
  25. Gottschick C., Deng Z.L., Vital M., Masur C., Abels C., Pieper D.H., Wagner-Döbler I. The urinary microbiota of men and women and its changes in women during bacterial vaginosis and antibiotic treatment. Microbiome. 2017; 5(1): 99. https://dx.doi.org/10.1186/s40168-017-0305-3.
  26. Fouts D.E., Pieper R., Szpakowski S., Pohl H., Knoblach S., Suh M.J. et al. Integrated next-generation sequencing of 16S rDNA and metaproteomics differentiate the healthy urine microbiome from asymptomatic bacteriuria in neuropathic bladder associated with spinal cord injury. J. Transl. Med. 2012; 10: 174. https://dx.doi.org/10.1186/1479-5876-10-174.
  27. Kramer H., Kuffel G., Thomas-White K., Wolfe A.J., Vellanki K., Leehey D.J. et al. Diversity of the midstream urine microbiome in adults with chronic kidney disease. Int. Urol. Nephrol. 2018; 50(6): 1123-30. https://dx.doi.org/10.1007/s11255-018-1860-7.
  28. Jacobs K.M., Price T.K., Thomas-White K., Halverson T., Davies A., Myers D.L., Wolfe A.J. Cultivable bacteria in urine of women with interstitial cystitis: (Not) What we expected. Female Pelvic Med. Reconstr. Surg. 2021; 27(5): 322-7. https://dx.doi.org/10.1097/SPV.0000000000000854.
  29. Putonti C., Thomas-White K., Crum E., Hilt E.E., Price T.K., Wolfe A.J. Genome investigation of urinary Gardnerella strains and their relationship to isolates of the vaginal microbiota. mSphere. 2021; 6(3): e00154-21. https://dx.doi.org/10.1128/mSphere.00154-21.
  30. Ravel J., Gajer P., Abdo Z., Schneider G.M., Koenig S.S., McCulle S.L. et al. Vaginal microbiome of reproductive-age women. Proc. Natl. Acad. Sci. USA. 2011; 108 (Suppl.1): 4680-7. https://dx.doi.org/10.1073/pnas.1002611107.
  31. Czaja C.A., Stamm W.E., Stapleton A.E., Roberts P.L., Hawn T.R., Scholes D. et al. Prospective cohort study of microbial and inflammatory events immediately preceding Escherichia coli recurrent urinary tract infection in women. J. Infect. Dis. 2009; 200(4): 528-36. https://dx.doi.org/10.1086/600385.
  32. Park M.G., Cho S., Oh M.M. Menopausal changes in the microbiome-a review focused on the genitourinary microbiome. Diagnostics (Basel). 2023; 13(6): 1193. https://dx.doi.org/10.3390/diagnostics13061193.
  33. Кира Е.Ф., Припутневич Т.В., Муравьева В.В., Халтурина Ю.В. Трансплантация вагинальной микробиоты. Акушерство и гинекология. 2023; 10: 39-46. [Kira E.F., Priputnevich T.V., Muravieva V.V., Khalturina Yu.V. Vaginal microbiota transplantation. Obstetrics and Gynecology. 2023; (10): 39-46. (in Russian)]. https://dx.doi.org/10.18565/aig.2023.142.
  34. Stapleton A.E. The vaginal microbiota and urinary tract infection. Microbiol. Spectr. 2016; 4(6):10.1128/microbiolspec.UTI-0025-2016. https://dx.doi.org/10.1128/microbiolspec.UTI-0025-2016.
  35. Govender Y., Gabriel I., Minassian V., Fichorova R. The current evidence on the association between the urinary microbiome and urinary incontinence in women. Front. Cell. Infect. Microbiol. 2019; 9: 133. https://dx.doi.org/10.3389/fcimb.2019.00133.
  36. Ammitzbøll N., Bau B.P.J., Bundgaard-Nielsen C., Villadsen A.B., Jensen A.M., Leutscher P.D.C. et al. Pre- and postmenopausal women have different core urinary microbiota. Sci. Rep. 2021; 11(1): 2212. https://dx.doi.org/10.1038/s41598-021-81790-8.
  37. Набока Ю. Л., Рымашевский А. Н., Коган М. И., Гудима И.А., Боровлева О.А., Джалагония К.Т., Заруцкий С.А. Микробиота мочи и влагалища здоровых женщин постменопаузального возраста (пилотное исследование). Урология. 2016; 1:18-24. [Naboka Yu.L., Rymashevsky A.N., Kogan M.I., Gudima I.A., Borovleva O.A., Jalagonia K.T., Zarutskiy S.A. Microbiota of urine and vagina of healthy postmenopausal women (a pilot study). Urologiia. 2016; (1): 18-24. (in Russian)].
  38. Curtiss N., Balachandran A., Krska L., Peppiatt-Wildman C., Wildman S., Duckett J. Age, menopausal status and the bladder microbiome. Eur. J. Obstet. Gynecol. Reprod. Biol. 2018; 228: 126-9. https://dx.doi.org/10.1016/j.ejogrb.2018.06.011.
  39. Hugenholtz F., van der Veer C., Terpstra M.L., Borgdorff H., van Houdt R., Bruisten S. et al. Urine and vaginal microbiota compositions of postmenopausal and premenopausal women differ regardless of recurrent urinary tract infection and renal transplant status. Sci. Rep. 2022; 12(1): 2698. https://dx.doi.org/10.1038/s41598-022-06646-1.
  40. Bjorling D.E., Wang Z.Y. Estrogen and neuroinflammation. Urology. 2001; 57(6, Suppl. 1): 40-6. https://dx.doi.org/10.1016/s0090-4295(01)01124-4.
  41. Irwin D.E., Milsom I., Hunskaar S., Reilly K., Kopp Z., Herschorn S. et al. Population-based survey of urinary incontinence, overactive bladder, and other lower urinary tract symptoms in five countries: results of the EPIC study. Eur. Urol. 2006; 50(6): 1306-14. https://dx.doi.org/10.1016/j.eururo.2006.09.019.
  42. Peyronnet B., Mironska E., Chapple C., Cardozo L., Oelke M., Dmochowski R. et al. A comprehensive review of overactive bladder pathophysiology: on the way to tailored treatment. Eur. Urol. 2019; 75(6): 988-1000. https://dx.doi.org/10.1016/j.eururo.2019.02.038.
  43. Deen N.S., Ahmed A., Tasnim N.T., Khan N. Clinical relevance of expanded quantitative urine culture in health and disease. Front. Cell. Infect. Microbiol. 2023; 13: 1210161. https://dx.doi.org/10.3389/fcimb.2023.1210161.
  44. Ковалев Г.В., Шкарупа Д.Д., Зайцева А.О., Старосельцева O.Ю., Бородулина И.В., Калинина Д.С., Мусиенко П.Е. Особенности клеточной регуляции нижних мочевыводящих путей как причина гиперактивности мочевого пузыря и снижения эффективности медикаментозной терапии. Урология. 2020; 5: 149-56. [Kovalev G.V., Shkarupa D.D., Zaytseva A.O., Staroseltseva O.Y., Borodulina I.V., Kalinina D.S., Musienko P.E. Cellular regulation of the lower urinary tract as a cause of the bladder overactivity and reduced efficiency of pharmacotherapy. Urologiia. 2020; (5): 149-56. (in Russian)]. https://dx.doi.org/10.18565/urology.2020.5.149-156.
  45. Mansfield K.J., Chen Z., Moore K.H., Grundy L. Urinary tract infection in overactive bladder: an update on pathophysiological mechanisms. Front. Physiol. 2022; 13: 886782. https://dx.doi.org/10.3389/fphys.2022.886782.
  46. Uhlig F., Grundy L., Garcia-Caraballo S., Brierley S.M., Foster S.J., Grundy D. Identification of a quorum sensing-dependent communication pathway mediating bacteria-gut-brain cross talk. iScience. 2020; 23(11): 101695. https://dx.doi.org/10.1016/j.isci.2020.101695.
  47. Yang N.J., Chiu I.M. Bacterial signaling to the nervous system through toxins and metabolites. J. Mol. Biol. 2017; 429(5): 587-605. https://dx.doi.org/10.1016/j.jmb.2016.12.023.
  48. Павлова И.В., Бердичевский В.Б., Сапоженкова Е.В., Гоняев А.Р., Болдырев А.Л., Петров Д.И., Хилькевич Е.С., Ахундов Э.Ф. Микробиота и функциональное состояние мочевых путей (обзор литературы). Бюллетень медицинской науки. 2023; 30(2): 99-105. [Pavlova I.V., Berdichevsky V.B., Sapozhenkova E.V., Gonyaev A.R., Boldyrev A.J., Petrov D.I., Khilkevich E.S., Akhundov E.F. Microbiota and urinary tract function: a comprehensive literature review. Bulletin of Medical Science. 2023; 30(2): 99-105. (in Russian)]. https://dx.doi.org/10.31684/25418475-2023-2-99.
  49. Thomas-White K.J., Kliethermes S., Rickey L., Lukacz E.S., Richter H.E., Moalli P. et al. National Institute of Diabetes and Digestive and Kidney Diseases Urinary Incontinence Treatment Network. Evaluation of the urinary microbiota of women with uncomplicated stress urinary incontinence. Am. J. Obstet. Gynecol. 2017; 216(1): 55.e1-55.e16. https://dx.doi.org/10.1016/j.ajog.2016.07.049.
  50. Price T.K., Lin H., Gao X., Thomas-White K.J., Hilt E.E., Mueller E.R., Wolfe A.J. et al. Bladder bacterial diversity differs in continent and incontinent women: a cross-sectional study. Am. J. Obstet. Gynecol. 2020; 223(5): 729.e1-729.e10. https://dx.doi.org/ 10.1016/j.ajog.2020.04.033.
  51. Halverson T., Mueller E.R., Brubaker L., Wolfe A.J. Symptom improvement with mirabegron treatment is associated with urobiome changes in adult women. Int. Urogynecol. J. 2022; 33(5): 1319-28. https://dx.doi.org/10.1007/s00192-022-05190-w.

Received 19.12.2023

Accepted 01.02.2024

About the Authors

Lev E. Belyi, Dr. Med. Sci., Professor of the Department of hospital surgery, anesthesiology, reanimatology, urology, traumatology, orthopedics, Ulyanovsk State University, 432017, Russia, Ulyanovsk, Leo Tolstoy str., 42, +7(917)605-97-19, lbely@yandex.ru, https://orcid.org/0000-0003-0908-1321

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